Cells of renin lineage take on a podocyte phenotype in aging nephropathy

American Journal of Physiology - Renal Physiology

Volumn 306, Issue 10, 2014, Pages

  Pippin, Jeffrey W ^a   Glenn, Sean T ^b   Krofft, Ronald D ^a   Rusiniak, Michael E ^b   Alpers, Charles E ^c   Hudkins, Kelly ^c   Duffield, Jeremy S ^a   Gross, Kenneth W ^b   Shankland, Stuart J ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cells of renin lineage; Focal segmental glomerulosclerosis; Glomerulus; Podocyte; Regeneration

Indexed keywords

NEPHRIN; PODOCIN; RENIN; SYNAPTOPODIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; GENE MAPPING; GLOMERULUS; GLOMERULUS BASEMENT MEMBRANE; KIDNEY CELL; KIDNEY DISEASE; KIDNEY INJURY; MOUSE; NONHUMAN; PHENOTYPE; PODOCYTE; PRIORITY JOURNAL; STEM CELL; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR SMOOTH MUSCLE;

CELLS OF RENIN LINEAGE; FOCAL SEGMENTAL GLOMERULOSCLEROSIS; GLOMERULUS; PODOCYTE; REGENERATION;

AGING; ANIMALS; CELL COUNT; CELL LINE; CELL LINEAGE; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; KIDNEY GLOMERULUS; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; PODOCYTES; RENIN;

EID: 84900820000     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00699.2013     Document Type: Article

References (61)

1. Ahn SY, Ryu J, Baek SH, Kim S, Na KY, Kim KW, Chae DW, Chin HJ. Incident chronic kidney disease and newly developed complications related to renal dysfunction in an elderly population during 5 years: a community-based elderly population cohort study. PLos One 8: e84467, 2013.
2. Alpers CE, Hudkins KL, Floege J, Johnson RJ. Human renal cortical interstitial cells with some features of smooth muscle cells participate in tubulointerstitial and crescentic glomerular injury. J Am Soc Nephrol 5: 201-209, 1994.
3. Angelotti ML, Lazzeri E, Lasagni L, Romagnani P. Only anti-CD133 antibodies recognizing the CD133/1 or the CD133/2 epitopes can identify human renal progenitors. Kidney Int 78: 620-621, 2010.
4. Benigni A, Morigi M, Rizzo P, Gagliardini E, Rota C, Abbate M, Ghezzi S, Remuzzi A, Remuzzi G. Inhibiting angiotensin-converting enzyme promotes renal repair by limiting progenitor cell proliferation and restoring the glomerular architecture. Am J Pathol 179: 628-638, 2011.
5. Brinkkoetter PT, Wu JS, Ohse T, Krofft RD, Schermer B, Benzing T, Pippin JW, Shankland SJ. p35, the non-cyclin activator of Cdk5, protects podocytes against apoptosis in vitro and in vivo. Kidney Int 77: 690-699, 2010.
6. Conti S, Cassis P, Benigni A. Aging and the renin-angiotensin system. Hypertension 60: 878-883, 2012.
7. Durvasula RV, Shankland SJ. Activation of a local renin angiotensin system in podocytes by glucose. Am J Physiol Renal Physiol 294: F830-F839, 2008.
8. Fukuda A, Chowdhury MA, Venkatareddy MP, Wang SQ, Nishizono R, Suzuki T, Wickman LT, Wiggins JE, Muchayi T, Fingar D, Shedden KA, Inoki K, Wiggins RC. Growth-dependent podocyte failure causes glomerulosclerosis. J Am Soc Nephrol 23: 1351-1363, 2012.
9. Glassock RJ. An update on glomerular disease in the elderly. Clin Geriatric Med 29: 579-591, 2013.
10. Glassock RJ, Rule AD. The implications of anatomical and functional changes of the aging kidney: with an emphasis on the glomeruli. Kidney Int 82: 270-277, 2012.
11. Gomez RA, Belyea B, Medrano S, Pentz ES, Sequeira-Lopez ML. Fate and plasticity of renin precursors in development and disease. Pediatr Nephrol 29: 721-726, 2014.
12. Grahammer F, Wanner N, Huber TB. Podocyte regeneration: who can become a podocyte? Am J Pathol 183: 333-335, 2013.
13. Griffin SV, Petermann AT, Durvasula RV, Shankland SJ. Podocyte proliferation and differentiation in glomerular disease: role of cell-cycle regulatory proteins. Nephrol Dial Transplant 18, Suppl 6: vi8-13, 2003.
14. Hackl MJ, Burford JL, Villanueva K, Lam L, Susztak K, Schermer B, Benzing T, Peti-Peterdi J. Tracking the fate of glomerular epithelial cells in vivo using serial multiphoton imaging in new mouse models with fluorescent lineage tags. Nat Med 19: 1661-1666, 2013.
15. Han XL, Liehr JG. Induction of covalent DNA adducts in rodents by tamoxifen. Cancer Res 52: 1360-1363, 1992.
16. Hugo C, Shankland SJ, Bowen-Pope DF, Couser WG, Johnson RJ. Extraglomerular origin of the mesangial cell after injury. A new role of the juxtaglomerular apparatus. J Clin Invest 100: 786-794, 1997.
17. Jarad G, Pippin JW, Shankland SJ, Kreidberg JA, Miner JH. Dystroglycan does not contribute significantly to kidney development or function, in health or after injury. Am J Physiol Renal Physiol 300: F811-F820, 2011.
18. Kitamura H, Shimizu A, Masuda Y, Ishizaki M, Sugisaki Y, Yamanaka N. Apoptosis in glomerular endothelial cells during the development of glomerulosclerosis in the remnant-kidney model. Exp Nephrol 6: 328-336, 1998.
19. Kriz W. The pathogenesis of "classic" focal segmental glomerulosclerosis-lessons from rat models. Nephrol Dial Transplant 18, Suppl 6: vi39-44, 2003.
20. Kriz W. Progressive renal failure-inability of podocytes to replicate and the consequences for development of glomerulosclerosis. Nephrol Dial Transplant 11: 1738-1742, 1996.
21. Kurt B, Paliege A, Willam C, Schwarzensteiner I, Schucht K, Neymeyer H, Sequeira-Lopez ML, Bachmann S, Gomez RA, Eckardt KU, Kurtz A. Deletion of von Hippel-Lindau protein converts reninproducing cells into erythropoietin-producing cells. J Am Soc Nephrol 24: 433-444, 2013.
22. Kurtz A. Control of renin synthesis and secretion. Am J Hypertens 25: 839-847, 2012.
23. Kurtz A. Renin release: sites, mechanisms, control. Annu Rev Physiol 73: 377-399, 2011.
24. Kusaba T, Lalli M, Kramann R, Kobayashi A, Humphreys BD. Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci USA 111: 1527-1532, 2014.
25. Lasagni L, Ballerini L, Angelotti ML, Parente E, Sagrinati C, Mazzinghi B, Peired A, Ronconi E, Becherucci F, Bani D, Gacci M, Carini M, Lazzeri E, Romagnani P. Notch activation differentially regulates renal progenitors proliferation and differentiation toward the podocyte lineage in glomerular disorders. Stem Cells 28: 1674-1685, 2010.
26. Lasagni L, Romagnani P. Basic research: podocyte progenitors and ectopic podocytes. Nat Rev Nephrol 9: 715-716, 2013.
27. Lee LK, Meyer TW, Pollock AS, Lovett DH. Endothelial cell injury initiates glomerular sclerosis in the rat remnant kidney. J Clin Invest 96: 953-964, 1995.
28. Matsusaka T, Xin J, Niwa S, Kobayashi K, Akatsuka A, Hashizume H, Wang QC, Pastan I, Fogo AB, Ichikawa I. Genetic engineering of glomerular sclerosis in the mouse via control of onset and severity of podocyte-specific injury. J Am Soc Nephrol 16: 1013-1023, 2005.
29. Miyazaki Y, Shimizu A, Ichikawa I, Hosoya T, Pastan I, Matsusaka T. Mice are unable to endogenously regenerate podocytes during the repair of immunotoxin-induced glomerular injury. Nephrol Dial Transplant. [Epub ahead of print].
30. Peired A, Angelotti ML, Ronconi E, la Marca G, Mazzinghi B, Sisti A, Lombardi D, Giocaliere E, Della Bona M, Villanelli F, Parente E, Ballerini L, Sagrinati C, Wanner N, Huber TB, Liapis H, Lazzeri E, Lasagni L, Romagnani P. Proteinuria impairs podocyte regeneration by sequestering retinoic acid. J Am Soc Nephrol 24: 1756-1768, 2013.
31. Perico N, Remuzzi G, Benigni A. Aging and the kidney. Curr Opin Nephrol Hypertens 20: 312-317, 2011.
32. Phillips LM, Wang Y, Dai T, Feldman DL, LaPage J, Adler SG. The renin inhibitor aliskiren attenuates high-glucose induced extracellular matrix synthesis and prevents apoptosis in cultured podocytes. Nephron Exp Nephrol 118: e49-59, 2011.
33. Pichaiwong W, Hudkins KL, Wietecha T, Nguyen TQ, Tachaudomdach C, Li W, Askari B, Kobayashi T, O'Brien KD, Pippin JW, Shankland SJ, Alpers CE. Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. J Am Soc Nephrol 24: 1088-1102, 2013.
34. Pippin JW, Sparks MA, Glenn ST, Buitrago S, Coffman TM, Duffield JS, Gross KW, Shankland SJ. Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease. Am J Pathol 183: 542-557, 2013.
35. Raveh-Amit H, Berzsenyi S, Vas V, Ye D, Dinnyes A. Tissue resident stem cells: till death do us part. Biogerontology 14: 573-590, 2013.
36. Rizzo P, Perico N, Gagliardini E, Novelli R, Alison MR, Remuzzi G, Benigni A. Nature and mediators of parietal epithelial cell activation in glomerulonephritides of human and rat. Am J Pathol 183: 1769-1778, 2013.
37. Rohani L, Johnson AA, Arnold A, Stolzing A. The aging signature: a hallmark of iPS cells? Aging Cell 2013.
38. Romagnani P, Lasagni L, Remuzzi G. Renal progenitors: an evolutionary conserved strategy for kidney regeneration. Nat Rev Nephrol 9: 137-146, 2013.
39. Romagnani P, Remuzzi G. Renal progenitors in non-diabetic and diabetic nephropathies. Trends Endocrinol Metab 24: 13-20, 2013.
40. Rosenberg ME, Correa-Rotter R, Inagami T, Kren SM, Hostetter TH. Glomerular renin synthesis and storage in the remnant kidney in the rat. Kidney Int 40: 677-683, 1991.
41. Rosner M, Abdel-Rahman E, Williams ME, ASN Advisory Group on Geriatric Nephrology. Geriatric nephrology: responding to a growing challenge. Clin J Am Soc Nephrol 5: 936-942, 2010.
42. Sakamoto K, Ueno T, Kobayashi N, Hara S, Takashima Y, Pastan I, Matsusaka T, Nagata M. The direction and role of phenotypic transition between podocytes and parietal epithelial cells in focal segmental glomerulosclerosis. Am J Physiol Renal Physiol 306: F98-F104, 2014.
43. Schulte K, Berger K, Boor P, Jirak P, Gelman IH, Arkill KP, Neal CR, Kriz W, Floege J, Smeets B, Moeller MJ. Origin of parietal podocytes in atubular glomeruli mapped by lineage tracing. J Am Soc Nephrol 25: 129-141, 2014.
44. Schwartz MM, Evans J, Bidani AK. The mesangium in the long-term remnant kidney model. J Lab Clin Med 124: 644-651, 1994.
45. Sequeira Lopez ML, Pentz ES, Nomasa T, Smithies O, Gomez RA. Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened. Dev Cell 6: 719-728, 2004.
46. Shankland SJ, Hamel P, Scholey JW. Cyclin and cyclin-dependent kinase expression in the remnant glomerulus. J Am Soc Nephrol 8: 368-375, 1997.
47. Shankland SJ, Smeets B, Pippin JW, Moeller MJ. The emergence of the glomerular parietal epithelial cell. Nat Rev Nephrol 10: 158-173, 2014.
48. Smeets B, Angelotti ML, Rizzo P, Dijkman H, Lazzeri E, Mooren F, Ballerini L, Parente E, Sagrinati C, Mazzinghi B, Ronconi E, Becherucci F, Benigni A, Steenbergen E, Lasagni L, Remuzzi G, Wetzels J, Romagnani P. Renal progenitor cells contribute to hyperplastic lesions of podocytopathies and crescentic glomerulonephritis. J Am Soc Nephrol 20: 2593-2603, 2009.
49. Taniguchi Y, Pippin JW, Hagmann H, Krofft RD, Chang AM, Zhang J, Terada Y, Brinkkoetter P, Shankland SJ. Both cyclin I and p35 are required for maximal survival benefit of cyclin-dependent kinase 5 in kidney podocytes. Am J Physiol Renal Physiol 302: F1161-F1171, 2012.
50. Tonelli M, Riella MC. Chronic kidney disease and the aging population. Kidney Int 85: 487-491, 2014.
51. Urruticoechea A, Smith IE, Dowsett M. Proliferation marker Ki-67 in early breast cancer. J Clin Oncol 23: 7212-7220, 2005.
52. Wanner N, Hartleben B, Herbach N, Goedel M, Stickel N, Zeiser R, Walz G, Moeller MJ, Grahammer F, Huber TB. Unraveling the role of podocyte turnover in glomerular aging and injury. J Am Soc Nephrol 25: 707-716, 2014.
53. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, Saunders TL, Dysko RC, Kohno K, Holzman LB, Wiggins RC. Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol 16: 2941-2952, 2005.
54. Wiggins J. Podocytes and glomerular function with aging. Semin Nephrol 29: 587-593, 2009.
55. Wiggins J, Bitzer M. Slowing the aging process. Clin Geriatric Med 29: 721-730, 2013.
56. Wiggins JE. Aging in the glomerulus. J Gerontol A Biol Sci Med Sci 67: 1358-1364, 2012.
57. Wiggins JE, Goyal M, Sanden SK, Wharram BL, Shedden KA, Misek DE, Kuick RD, Wiggins RC. Podocyte hypertrophy, "adaptation, " and "decompensation" associated with glomerular enlargement and glomerulosclerosis in the aging rat: prevention by calorie restriction. J Am Soc Nephrol 16: 2953-2966, 2005.
58. Wiggins RC. The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int 71: 1205-1214, 2007.
59. Zhang J, Hansen KM, Pippin JW, Chang AM, Taniguchi Y, Krofft RD, Pickering SG, Liu Z, Abrass CK, Shankland SJ. De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy. Am J Physiol Renal Physiol 302: F571-F580, 2012.
60. Zhang J, Pippin JW, Krofft RD, Naito S, Liu Z, Shankland SJ. Podocyte repopulation by renal progenitor cells following glucocorticoids treatment in experimental FSGS. Am J Physiol Renal Physiol 304: F1375-F1389, 2013.
61. Zhang J, Pippin JW, Vaughan MR, Krofft RD, Taniguchi Y, Romagnani P, Nelson PJ, Liu ZH, Shankland SJ. Retinoids augment the expression of podocyte proteins by glomerular parietal epithelial cells in experimental glomerular disease. Nephron Exp Nephrol 121: e23-e37, 2012.